Support for Golgi maturation theory

Two studies demonstrate that individual Golgi cisternae mature from early to late, potentially resolving long debate

By Juhi Yajnik | May 15, 2006

Individual Golgi compartments mature, report two teams of scientists working independently, perhaps resolving a controversy that has lingered in cell biology for decades. The studies, published this week in Nature, report observations of Golgi cisternae transitioning from early (cis) to late (trans) in the yeast Saccharomyces cerevisiae, suggesting that proteins remain within a single cisterna before being secreted.
"How things move within the Golgi is one of the most contentious issues of membrane biology in the modern era," said Randy Schekman, professor of cell biology at the University of California, Berkeley, who was not involved with the studies. Both groups "developed the technology to visualize what happens in a membrane stack."
Currently, some cell biology textbooks teach two models of Golgi maturation. One model, sometimes called the traditional model, suggests the cisternae -- membrane sacs of the secretory pathway -- don't mature. Each cisterna has a specific set of enzymes, and cargo proteins ride in vesicles from sac to sac, being modified along the way until they are secreted.
While there is experimental evidence for the traditional model, scientists have discovered some algae that have enormous scales. These scales are made within the Golgi apparatus, but are too big to be transported within vesicles.
This finding helped to rekindle the cisternal maturation model, which suggests that a single Golgi compartment changes from early to late, enabling cargo proteins to reside within the same maturing cisterna until they are ready to pass through the plasma membrane. In this model, the large algal scales would just stay in one Golgi membrane compartment, while the enzymes around them changed. But scientists needed evidence that this maturation occurred. "It's a fairly obvious question," said Benjamin Glick from the University of Chicago, lead author of one of the studies. "Is there a way to see this maturation occur?"
Golgi cisternae are tightly stacked and difficult to differentiate using microscopy, frustrating early visualization efforts in most model organisms. Both groups, however, used S. cerevisiae, whose composition of Golgi membranes resembles that in mammals. However, this yeast's Golgi compartments are not stacked, and instead float individually within the cell, making it easier to distinguish what's happening where.
Glick and his team tagged early Golgi proteins with green fluorescent protein (GFP), and then tagged the late-Golgi proteins with a different fluorescent protein, DsRed. They showed that each Golgi cisterna began with green fluorescence and then gradually glowed red -- compelling evidence for the cisternal maturation model.
In the other study, Akihiko Nakano of the RIKEN Discovery Research Institute and University of Tokyo in Japan and colleagues also tagged Golgi proteins with GFP and a red marker, red fluorescent protein (mRFP). They observed a similar color pattern over time.
Glick and his team also found that Golgi cisternae mature within four to six minutes, ample time for many proteins to travel from the ER to the plasma membrane.
"The results are clean and provide support to the proposal of cisternal maturation," Vivek Malhotra at the University of California, San Diego, who was not involved with the studies, said in an Email to The Scientist. Still, he added that "a number of issues" need to be addressed. For instance, given the differences between the Golgi in S. cerevisiae and other species, Malhotra wondered if they share the same mechanism for transporting proteins between the cisternae.
Glick agreed that the process of Golgi maturation is still "mysterious." For instance, it's unclear which protein pathways are used, how resident Golgi proteins recycle from late back to early cisternae, and what regulates the system. Still, he said that these results are significant. "For anyone thinking about the Golgi, changes to the Golgi model influence every aspect of the way you think about this organelle."
Juhi Yajnik
Juhi.Yajnik@gmail.com
Links within this article
E. Losev et al, "Golgi maturation visualized in living yeast," Nature, May 14, 2006.
http://www.nature.com
K. Matsuura-Tokita, "Live imaging of yeast Golgi cisternal maturation," Nature, May 14, 2006.
http://www.nature.com
K. Hopkin, "Seeking accurate traffic reports," The Scientist, December 6, 2004.
http://www.the-scientist.com/article/display/15143/
Randy Schekman
http://mcb.berkeley.edu/labs/schekman/
Becker B et al, "The secretory pathway of protists: spatial and functional organization and evolution," Microbiological Reviews, December 1996.
PM_ID: 8987360
Benjamin Glick
http://cmp.bsd.uchicago.edu/faculty/bGlick.html
T. Toma, "The fluid structure of Golgi," The Scientist, November 16, 2001.
http://www.the-scientist.com/article/display/20036/
Ahikiko Nakano
http://db.yeastgenome.org/cgi-bin/colleague/colleagueSearch?id=4182
Vivek Malhotra
http://www-biology.ucsd.edu/faculty/malhotra.html